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New Light Shed on the Early Evolution of Limb-Bone Growth Plate and Bone Marrow

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New Light Shed on the Early Evolution of Limb-Bone Growth Plate and Bone Marrow RESEARCH ARTICLE New light shed on the early evolution of limb-bone growth plate and bone marrow Jordi Estefa1*, Paul Tafforeau2, Alice M Clement3, Jozef Klembara4, Grzegorz Niedz´wiedzki1, Camille Berruyer2, Sophie Sanchez1,2* 1Department of Organismal Biology, Evolution and Development, Uppsala University, Uppsala, Sweden; 2European Synchrotron Radiation Facility, Grenoble, France; 3Flinders University, College of Science and Engineering, Adelaide, Australia; 4Comenius University in Bratislava, Faculty of Natural Sciences, Department of Ecology, Bratislava, Slovakia Abstract The production of blood cells (haematopoiesis) occurs in the limb bones of most tetrapods but is absent in the fin bones of ray-finned fish. When did long bones start producing blood cells? Recent hypotheses suggested that haematopoiesis migrated into long bones prior to the water-to-land transition and protected newly-produced blood cells from harsher environmental conditions. However, little fossil evidence to support these hypotheses has been provided so far. Observations of the humeral microarchitecture of stem-tetrapods, batrachians, and amniotes were performed using classical sectioning and three-dimensional synchrotron virtual histology. They show that Permian tetrapods seem to be among the first to exhibit a centralised marrow organisation, which allows haematopoiesis as in extant amniotes. Not only does our study demonstrate that long-bone haematopoiesis was probably not an exaptation to the water-to-land transition but it sheds light on the early evolution of limb-bone development and the sequence of bone-marrow functional acquisitions. *For correspondence: [email protected] (JE); [email protected] (SS) Introduction Tetrapod long bones are among the most studied skeletal elements in the field of bone biology as Competing interests: The they constitute a unit of reference for understanding the development and biomechanics of the authors declare that no appendicular skeleton (e.g. Duboule, 1994; Fro¨bisch, 2008; Hall, 2008; Shubin et al., 1997). The competing interests exist. recent discovery of fossil tetrapod trackways (Ahlberg, 2018; Niedz´wiedzki et al., 2010) suggested Funding: See page 24 that limbs supported weight and engaged substrate locomotion earlier than previously thought in Received: 04 September 2019 early tetrapod evolution. Not only crucial for their biomechanical properties, long bones also host Accepted: 21 December 2020 bone marrow including stem-cell niches for the production of blood cells, that is haematopoiesis Published: 02 March 2021 (Orkin and Zon, 2008). After birth, bone marrow is the definitive haematopoietic system in mostly terrestrial mammals and many other tetrapods (Akiyoshi and Inoue, 2012; Kapp et al., 2018; Reviewing editor: Diethard Tautz, Max-Planck Institute for Orkin and Zon, 2008) but not in fish or some aquatic tetrapods (Akiyoshi and Inoue, 2012; Evolutionary Biology, Germany Avagyan and Zon, 2016; Kapp et al., 2018). Indeed, red blood cells are produced in the supraspi- nal organ in the lamprey, the kidney and liver in actinopterygians (ray-finned fish) and some amphib- Copyright Estefa et al. This ians (tadpoles and aquatic adults, Akiyoshi and Inoue, 2012), and the kidney in lungfish article is distributed under the (Amemiya et al., 2007; Kapp et al., 2018). Several studies proposed that the skeleton would have terms of the Creative Commons Attribution License, which played a major role in hosting blood-cell production over the water-to-land transition and (1) pro- permits unrestricted use and tecting it against temperature changes (Weiss and Wislocki, 1956), (2) protecting it against poten- redistribution provided that the tial DNA mutations induced by UV exposure on land (Horton, 1980; Kapp et al., 2018) or (3) original author and source are providing a better efficiency in red-blood-cell production necessary for metabolically-demanding ter- credited. restrial locomotion and aerial respiration (Tanaka, 1976). Our study focusses on characterising the Estefa et al. eLife 2021;10:e51581. DOI: https://doi.org/10.7554/eLife.51581 1 of 30 Research article Evolutionary Biology eLife digest For many aquatic creatures, the red blood cells that rush through their bodies are created in organs such as the liver or the kidney. In most land vertebrates however, blood-cell production occurs in the bone marrow. There, the process is shielded from the ultraviolet light or starker temperature changes experienced out of the water. It is possible that this difference evolved long before the first animal with a backbone crawled out of the aquatic environment and faced new, harsher conditions: yet very little fossil evidence exists to support this idea. A definitive answer demands a close examination of fossils from the water-to-land transition including lobe-finned fish and early limbed vertebrates. To support the production of red blood cells, their fin and limb bones would have needed an internal cavity that can house a specific niche that opens onto a complex network of blood vessels. To investigate this question, Estefa et al. harnessed the powerful x-ray beam produced by the European Synchrotron Radiation Facility and imaged the fin and limb bones from fossil lobe-finned fish and early limbed vertebrates. The resulting three-dimensional structures revealed spongy long bones with closed internal cavities where the bone marrow cells were probably entrapped. These could not have housed the blood vessels needed to create an environment that produces red blood cells. In fact, the earliest four-legged land animals Estefa et al. found with an open marrow cavity lived 60 million years after vertebrates had first emerged from the aquatic environment, suggesting that blood cells only began to be created in bone marrow after the water-to-land transition. Future work could help to pinpoint exactly when the change in blood cell production occurred, helping researchers to identify the environmental and biological factors that drove this change. early evolution of the bone marrow and long-bone growth in fossils to contextualise these hypotheses. Tetrapod long bones are regionalised in three parts mirrored from midshaft (Figure 1): (1) the middle of the shaft is called diaphysis; (2) the metaphyses are located at each extremity of the shaft Figure 1. Schematic drawing of the long-bone epiphyses of extant amniotes (A) and amphibians (B). Four conditions are figured here. They are separated by yellow dashed lines: A1, condition in crocodiles (interpreted from Haines, 1938); A2, condition in mammals at an early developmental stage before the appearance of the secondary ossification centre (Anderson and Shapiro, 2010; Tanaka, 1976); B1, condition in Triturus (Cynops) pyrrhogaster (Quilhac et al., 2014; Tanaka, 1976); B2, condition in Rana catesbeiana (Francillon, 1981; Tanaka, 1976). Abbreviations: c., cortex; Dia., diaphysis; e., endosteal bone; Epi., epiphysis; h.c., hypertrophied chondrocytes; Meta., metaphysis; m.p., marrow process; s., sinusoids; sept., septum; trab., trabeculae. Estefa et al. eLife 2021;10:e51581. DOI: https://doi.org/10.7554/eLife.51581 2 of 30 Research article Evolutionary Biology and (3) the epiphyses start above the ossification notch (i.e. where the cortical bone stops forming), extend beyond the metaphyses, and comprise one or more condyles in the case of concave articula- tions (Francillon-Vieillot et al., 1990). Long bones elongate from the growth plate, which is located in the metaphysis (Figure 1). In this region, the cartilage is progressively substituted with bone: this process is called endochondral ossification (Francillon-Vieillot et al., 1990; Hall, 2005). In extant amniotes, long-bone elongation results from the proliferation of longitudinal columns of hypertrophic cartilage cells, called hypertrophic chondrocytes (Francillon-Vieillot et al., 1990; Haines, 1942; Xie et al., 2020; Figure 1A). The latter express collagen type X which facilitates the calcification of the surrounding matrix (Gudmann and Karsdal, 2016; Lu¨llmann-Rauch, 2015). To do so, the hypertrophic chondrocytes secrete matrix vesicles containing calcium phosphate crystals (Amizuka, 2012; Anderson and Shapiro, 2010). The vesicles align longitudinally along the septa. The crystals penetrate the vesicle membranes to form stellate clusters of needle-shaped apatite in the extra cellular matrix (Amizuka, 2012). The mineralisation thus propagates following the longitu- dinal organisation of the septa (Amizuka, 2012; Anderson and Shapiro, 2010; Figure 1A). Blood vessels and marrow processes invade the growth plate along these columns of hypertrophic carti- lage (Lu¨llmann-Rauch, 2015; Figure 1A). Lytic enzymes secreted by the bone-marrow cells degrade the cartilage matrix, which is progressively substituted by bone deposition (Lu¨llmann-Rauch, 2015; Suzuki et al., 1981). Growth factors, such as the vascular endothelial growth factor (VEGF), trigger cartilage calcification and regulate endochondral ossification through stimulation of blood-vessel ingrowth into the diaphysis (Gerber et al., 1999). The lines of calcifying stellate clusters of crystals therefore form a scaffold for future trabecular bone deposition (Amizuka, 2012). This results in the formation of a bony mesh of longitudinal trabeculae (Figure 1A), which is progressively incorporated into the metaphysis where haematopoietic stem cell (HSC) niches (Figure 1A) are located (Calvi et al., 2003; Zhang et al., 2003) in the close vicinity of trabecular/endothelial
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